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Pumping iron: A multi-omics analysis of two extremophilic algae reveals iron economy management

Marine algae are responsible for half of the world's primary productivity, but this critical carbon sink is often constrained by insufficient iron. One species of marine algae, Dunaliella tertiolecta, is remarkable for its ability to maintain photosynthesis and thrive in low-iron environments....

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Autores principales: Davidi, Lital, Gallaher, Sean D., Ben-David, Eyal, Purvine, Samuel O., Fillmore, Thomas L., Nicora, Carrie D., Craig, Rory J., Schmollinger, Stefan, Roje, Sanja, Blaby-Haas, Crysten E., Auber, Robert P., Wisecaver, Jennifer H., Merchant, Sabeeha S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10372677/
https://www.ncbi.nlm.nih.gov/pubmed/37459532
http://dx.doi.org/10.1073/pnas.2305495120
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author Davidi, Lital
Gallaher, Sean D.
Ben-David, Eyal
Purvine, Samuel O.
Fillmore, Thomas L.
Nicora, Carrie D.
Craig, Rory J.
Schmollinger, Stefan
Roje, Sanja
Blaby-Haas, Crysten E.
Auber, Robert P.
Wisecaver, Jennifer H.
Merchant, Sabeeha S.
author_facet Davidi, Lital
Gallaher, Sean D.
Ben-David, Eyal
Purvine, Samuel O.
Fillmore, Thomas L.
Nicora, Carrie D.
Craig, Rory J.
Schmollinger, Stefan
Roje, Sanja
Blaby-Haas, Crysten E.
Auber, Robert P.
Wisecaver, Jennifer H.
Merchant, Sabeeha S.
author_sort Davidi, Lital
collection PubMed
description Marine algae are responsible for half of the world's primary productivity, but this critical carbon sink is often constrained by insufficient iron. One species of marine algae, Dunaliella tertiolecta, is remarkable for its ability to maintain photosynthesis and thrive in low-iron environments. A related species, Dunaliella salina Bardawil, shares this attribute but is an extremophile found in hypersaline environments. To elucidate how algae manage their iron requirements, we produced high-quality genome assemblies and transcriptomes for both species to serve as a foundation for a comparative multiomics analysis. We identified a host of iron-uptake proteins in both species, including a massive expansion of transferrins and a unique family of siderophore-iron-uptake proteins. Complementing these multiple iron-uptake routes, ferredoxin functions as a large iron reservoir that can be released by induction of flavodoxin. Proteomic analysis revealed reduced investment in the photosynthetic apparatus coupled with remodeling of antenna proteins by dramatic iron-deficiency induction of TIDI1, which is closely related but identifiably distinct from the chlorophyll binding protein, LHCA3. These combinatorial iron scavenging and sparing strategies make Dunaliella unique among photosynthetic organisms.
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spelling pubmed-103726772023-07-28 Pumping iron: A multi-omics analysis of two extremophilic algae reveals iron economy management Davidi, Lital Gallaher, Sean D. Ben-David, Eyal Purvine, Samuel O. Fillmore, Thomas L. Nicora, Carrie D. Craig, Rory J. Schmollinger, Stefan Roje, Sanja Blaby-Haas, Crysten E. Auber, Robert P. Wisecaver, Jennifer H. Merchant, Sabeeha S. Proc Natl Acad Sci U S A Biological Sciences Marine algae are responsible for half of the world's primary productivity, but this critical carbon sink is often constrained by insufficient iron. One species of marine algae, Dunaliella tertiolecta, is remarkable for its ability to maintain photosynthesis and thrive in low-iron environments. A related species, Dunaliella salina Bardawil, shares this attribute but is an extremophile found in hypersaline environments. To elucidate how algae manage their iron requirements, we produced high-quality genome assemblies and transcriptomes for both species to serve as a foundation for a comparative multiomics analysis. We identified a host of iron-uptake proteins in both species, including a massive expansion of transferrins and a unique family of siderophore-iron-uptake proteins. Complementing these multiple iron-uptake routes, ferredoxin functions as a large iron reservoir that can be released by induction of flavodoxin. Proteomic analysis revealed reduced investment in the photosynthetic apparatus coupled with remodeling of antenna proteins by dramatic iron-deficiency induction of TIDI1, which is closely related but identifiably distinct from the chlorophyll binding protein, LHCA3. These combinatorial iron scavenging and sparing strategies make Dunaliella unique among photosynthetic organisms. National Academy of Sciences 2023-07-17 2023-07-25 /pmc/articles/PMC10372677/ /pubmed/37459532 http://dx.doi.org/10.1073/pnas.2305495120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Davidi, Lital
Gallaher, Sean D.
Ben-David, Eyal
Purvine, Samuel O.
Fillmore, Thomas L.
Nicora, Carrie D.
Craig, Rory J.
Schmollinger, Stefan
Roje, Sanja
Blaby-Haas, Crysten E.
Auber, Robert P.
Wisecaver, Jennifer H.
Merchant, Sabeeha S.
Pumping iron: A multi-omics analysis of two extremophilic algae reveals iron economy management
title Pumping iron: A multi-omics analysis of two extremophilic algae reveals iron economy management
title_full Pumping iron: A multi-omics analysis of two extremophilic algae reveals iron economy management
title_fullStr Pumping iron: A multi-omics analysis of two extremophilic algae reveals iron economy management
title_full_unstemmed Pumping iron: A multi-omics analysis of two extremophilic algae reveals iron economy management
title_short Pumping iron: A multi-omics analysis of two extremophilic algae reveals iron economy management
title_sort pumping iron: a multi-omics analysis of two extremophilic algae reveals iron economy management
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10372677/
https://www.ncbi.nlm.nih.gov/pubmed/37459532
http://dx.doi.org/10.1073/pnas.2305495120
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